The miR-317 functions as a negative regulator of Toll immune response and influences Drosophila survival

Li, Ruimin; Huang, Y.; Zhang, Qi; Zhou, Hongjian; Park, Jin; Ma, Fei

doi:10.1016/j.dci.2019.01.012

Cited by 32 publications

(30 citation statements)

References 54 publications

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“…In recent years, with the development of the in silico miRNA identification platform such as mirMachine ( Cagirici et al, 2021 ), miRanda ( Rehmsmeier et al, 2004 ) and RNAhybrid ( Mohebbi et al, 2021 ), many miRNAs have been characterized from multiple organisms including plants, vertebrates and invertebrates following the integration of various tools in bioinformatics, genetics, molecular biology and biochemistry. In insects, miRNAs played indispensable roles in development ( Shen et al, 2020 ), behavior ( Niu et al, 2019 ), immunity ( Li R. et al, 2019 ), host-virus interaction ( Singh, 2020 ), and resistance to multiple insecticides ( Zhu et al, 2019 ; Li X. et al, 2020 ). In addition, the high-quality genome offers the opportunity to explore the putative biological function of identified miRNAs ( Robertson et al, 2018 ).…”

Section: Discussionmentioning

confidence: 99%

Profiling of MicroRNAs in Midguts of Plutella xylostella Provides Novel Insights Into the Bacillus thuringiensis Resistance

Yang

Lin

et al. 2021

Front. Genet.

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The diamondback moth (DBM), Plutella xylostella, one of the most destructive lepidopteran pests worldwide, has developed field resistance to Bacillus thuringiensis (Bt) Cry toxins. Although miRNAs have been reported to be involved in insect resistance to multiple insecticides, our understanding of their roles in mediating Bt resistance is limited. In this study, we constructed small RNA libraries from midguts of the Cry1Ac-resistant (Cry1S1000) strain and the Cry1Ac-susceptible strain (G88) using a high-throughput sequencing analysis. A total of 437 (76 known and 361 novel miRNAs) were identified, among which 178 miRNAs were classified into 91 miRNA families. Transcripts per million analysis revealed 12 differentially expressed miRNAs between the Cry1S1000 and G88 strains. Specifically, nine miRNAs were down-regulated and three up-regulated in the Cry1S1000 strain compared to the G88 strain. Next, we predicted the potential target genes of these differentially expressed miRNAs and carried out GO and KEGG pathway analyses. We found that the cellular process, metabolism process, membrane and the catalytic activity were the most enriched GO terms and the Hippo, MAPK signaling pathway might be involved in Bt resistance of DBM. In addition, the expression patterns of these miRNAs and their target genes were determined by RT-qPCR, showing that partial miRNAs negatively while others positively correlate with their corresponding target genes. Subsequently, novel-miR-240, one of the differentially expressed miRNAs with inverse correlation with its target genes, was confirmed to interact with Px017590 and Px007885 using dual luciferase reporter assays. Our study highlights the characteristics of differentially expressed miRNAs in midguts of the Cry1S1000 and G88 strains, paving the way for further investigation of miRNA roles in mediating Bt resistance.

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Section: Discussionmentioning

confidence: 99%

Profiling of MicroRNAs in Midguts of Plutella xylostella Provides Novel Insights Into the Bacillus thuringiensis Resistance

Yang

Lin

et al. 2021

Front. Genet.

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“…For instance, based on expression profiling and target prediction, microRNAs have been suggested to regulate gene expression in immune responses and pathways in the tobacco hornworm, honeybees, greater wax moth, and fruit fly [ 39 – 42 ]. Specifically, in fruit fly, microRNA-310 family members suppress the expression of Drosomysin, an AMP mediated by Toll signaling [ 43 ]; microRNA-317 directly targets the transcription factor Dif-Rc in the Toll pathway to down-regulate the expression of Drosomysin [ 44 ]. MicroRNA-9a and microRNA-981 target and repress the expression of AMP Diptericin, which is mediated by IMD signaling [ 45 ]; in contrast, microRNA-34 activates IMD signaling by repressing Eip75B , a negative regulator of the IMD pathway [ 46 ].…”

Section: Introductionmentioning

confidence: 99%

JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184

Liu

Zhao

et al. 2020

PLoS Pathog

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Different from holometabolous insects, the hemipteran species such as pea aphid Acyrthosiphon pisum exhibit reduced immune responses with the absence of the genes coding for antimicrobial peptide (AMP), immune deficiency (IMD), peptidoglycan recognition proteins (PGRPs), and other immune-related molecules. Prior studies have proved that phenoloxidase (PO)-mediated melanization, hemocyte-mediated phagocytosis, and reactive oxygen species (ROS) participate in pea aphid defense against bacterial infection. Also, the conserved signaling, Jun N-terminal kinase (JNK) pathway, has been suggested to be involved in pea aphid immune defense. However, the precise role of the JNK signaling, its interplay with other immune responses and its regulation in pea aphid are largely unknown. In this study, using in vitro biochemical assays and in vivo bioassays, we demonstrated that the JNK pathway regulated hemolymph PO activity, hydrogen peroxide concentration and hemocyte phagocytosis in bacteria infected pea aphids, suggesting that the JNK pathway plays a central role in regulating immune responses in pea aphid. We further revealed the JNK pathway is regulated by microRNA-184 in response to bacterial infection. It is possible that in common the JNK pathway plays a key role in immune system of hemipteran insects and microRNA-184 regulates the JNK pathway in animals.

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“…Recently, our group has performed a genome-wide miRNA screening to identify miRNAs regulating Drosophila Toll-mediated innate immune response, employing small-RNA seq and transgenic UAS-miRNA library [37]. Several potential miRNAs have been screened out, followed by in-depth exploration of their regulatory mechanism [35][36][37]. The current study found that the high-expression of miR-959-962 cluster in flies suppressed antibacterial defenses, evidenced by lower survival rate and a significant decrease of Drs expression in the presence of Gram-positive bacterial challenge.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, the nuclear translocation of the transcription factor Dif or Dorsal and its activation of AMP expression are an indispensable step of the Toll pathway response. miR-958 [35] and miR-317 [36] have been identified the direct binding with the 3 UTR of Dif-Ra/b/d and Dif-Rc transcripts, respectively, while miR-8 targets to the Dorsal mRNA [34]. Last but not least, miR-310-313 family and miR-964 could directly target to the AMP gene Drosomycin to inhibit its expression [37,38].…”

Section: Introductionmentioning

confidence: 99%

The Drosophila miR-959–962 Cluster Members Repress Toll Signaling to Regulate Antibacterial Defense during Bacterial Infection

Yao

Zhou

et al. 2021

IJMS

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MicroRNAs (miRNAs) are a class of ~22 nt non-coding RNA molecules in metazoans capable of down-regulating target gene expression by binding to the complementary sites in the mRNA transcripts. Many individual miRNAs are implicated in a broad range of biological pathways, but functional characterization of miRNA clusters in concert is limited. Here, we report that miR-959–962 cluster (miR-959/960/961/962) can weaken Drosophila immune response to bacterial infection evidenced by the reduced expression of antimicrobial peptide Drosomycin (Drs) and short survival within 24 h upon infection. Each of the four miRNA members is confirmed to contribute to the reduced Drs expression and survival rate of Drosophila. Mechanically, RT-qPCR and Dual-luciferase reporter assay verify that tube and dorsal (dl) mRNAs, key components of Toll pathway, can simultaneously be targeted by miR-959 and miR-960, miR-961, and miR-962, respectively. Furthermore, miR-962 can even directly target to the 3′ untranslated region (UTR) of Toll. In addition, the dynamic expression pattern analysis in wild-type flies reveals that four miRNA members play important functions in Drosophila immune homeostasis restoration at the late stage of Micrococcus luteus (M. luteus) infection. Taken together, our results identify four miRNA members from miR-959–962 cluster as novel suppressors of Toll signaling and enrich the repertoire of immune-modulating miRNA in Drosophila.

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The miR-317 functions as a negative regulator of Toll immune response and influences Drosophila survival

Cited by 32 publications

References 54 publications

Profiling of MicroRNAs in Midguts of Plutella xylostella Provides Novel Insights Into the Bacillus thuringiensis Resistance

Profiling of MicroRNAs in Midguts of Plutella xylostella Provides Novel Insights Into the Bacillus thuringiensis Resistance

JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184

The Drosophila miR-959–962 Cluster Members Repress Toll Signaling to Regulate Antibacterial Defense during Bacterial Infection

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